Phenolic characterization and variability in leaves, stems and roots of Micro-Tom and patio tomatoes, in response to nitrogen limitation

Plant Science

Volumn 224, Issue , 2014, Pages 62-73

  Larbat, Romain ^a,b   Paris, Cédric ^c   Le Bot, Jacques ^d   Adamowicz, Stéphane ^d  

^a UNIVERSITÉ DE LORRAINE   (France)

^b UNIVERSITÉ DE LORRAINE   (France)

^c UNIVERSITÉ DE LORRAINE   (France)

^d Domaine Saint Paul   (France)

Author keywords

Flavonoids; Micro Tom; Phenolamides; Phenolic compounds; Solanum lycopersicum L.

Indexed keywords

ANTHOCYANIN; FLAVONOID; NITROGEN; PHENOL DERIVATIVE;

DEFICIENCY; METABOLISM; PLANT LEAF; PLANT ROOT; PLANT STEM; TOMATO;

ANTHOCYANINS; FLAVONOIDS; LYCOPERSICON ESCULENTUM; NITROGEN; PHENOLS; PLANT LEAVES; PLANT ROOTS; PLANT STEMS;

EID: 84899836581     PISSN: 01689452     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.plantsci.2014.04.010     Document Type: Article

References (87)

1. Hoffland E., Dicke M., Van Tintelen W., Dijkman H., Van Beusichem M.L. Nitrogen availability and defense of tomato against two-spotted spider mite. J. Chem. Ecol. 2000, 26:2697-2711.
2. Leser C., Treutter D. Effects of nitrogen supply on growth, contents of phenolic compounds and pathogen (scab) resistance of apple trees. Physiol. Plant. 2005, 123:49-56.
3. 2 concentrations leads to modified profiles of secondary metabolites in tobacco cv. SamsunNN and to increased resistance against infection with Potato virus Y. Plant Cell Environ. 2006, 29:126-137.
4. Niggeweg R., Michael A.J., Martin C. Engineering plants with increased levels of the antioxidant chlorogenic acid. Nat. Biotechnol. 2004, 22:746-754.
5. Leiss K.A., Choi Y.H., Abdel-Farid I.B., Verpoorte R., Klinkhamer P.G.L. NMR metabolomics of thrips (Frankliniella occidentalis) resistance in Senecio hybrids. J. Chem. Ecol. 2009, 35:219-229.
6. Leiss K.A., Maltese F., Choi Y.H., Verpoorte R., Klinkhamer P.G.L. Identification of chlorogenic acid as a resistance factor for thrips in Chrysanthemum. Plant Physiol. 2009, 150:1567-1575.
7. Kröner A., Marnet N., Andrivon D., Val F. Nicotiflorin, rutin and chlorogenic acid: phenylpropanoids involved differently in quantitative resistance of potato tubers to biotrophic and necrotrophic pathogens. Plant Physiol. Biochem. 2012, 57:23-31.
8. Hanson P.M., Yang R.Y., Wu J., Chen J.T., Ledesma D., Tsou S.C.S., Lee T.C. Variation for antioxidant activity and antioxidants in tomato. J. Am. Soc. Hortic. Sci. 2004, 129:704-711.
9. Carbone F., Preuss A., De Vos R.C.H., D'Amico E., Perrotta G., Bovy A.G., Martens S., Rosati C. Developmental, genetic and environmental factors affect the expression of flavonoid genes, enzymes and metabolites in strawberry fruits. Plant Cell Environ. 2009, 32:1117-1131.
10. Joet T., Salmona J., Laffargue A., Descroix F., Dussert S. Use of the growing environment as a source of variation to identify the quantitative trait transcripts and modules of co-expressed genes that determine chlorogenic acid accumulation. Plant Cell Environ. 2010, 33:1220-1233.
11. Koncic M.Z., Kremer D., Gruz J., Strand M., Bisevac G., Kosalec I., Samec D., Piljac-Zegara J., Karlovic K. Antioxidant and antimicrobial properties of Moltkia petraea (Tratt.) Griseb flower, leaf and stem infusions. Food Chem. Toxicol. 2010, 48:1537-1542.
12. Olsen K.M., Hehn A., Jugde H., Slimestad R., Larbat R., Bourgaud F., Lillo C. Identification and characterisation of CYP75A31, a new flavonoid 3'5'-hydroxylase, isolated from Solanum lycopersicum. BMC Plant Biol. 2010, 10:21.
13. Larsson S., Wirén A., Lundgren L., Ericsson T. Effects of light and nutrient stress on leaf phenolic chemistry in Salix dasyclados and susceptibility to Galerucella lineola (Coleoptera). Oikos 1986, 47:205-210.
14. Løvdal T., Olsen K.M., Slimestad R., Verheul M., Lillo C. Synergetic effects of nitrogen depletion, temperature, and light on the content of phenolic compounds and gene expression in leaves of tomato. Phytochemistry 2010, 71:605-613.
15. Wilkens R.T., Spoerke J.M., Stamp N.E. Differential responses of growth and two soluble phenolics of tomato to resource availability. Ecology 1996, 77:247-258.
16. Fritz C., Palacios-Rojas N., Feil R., Stitt M. Regulation of secondary metabolism by the carbon-nitrogen status in tobacco: nitrate inhibits large sectors of phenylpropanoid metabolism. Plant J. 2006, 46:533-548.
17. Larbat R., Le Bot J., Bourgaud F., Robin C., Adamowicz S. Organ-specific responses of tomato growth and phenolic metabolism to nitrate limitation. Plant Biol. 2012, 14:760-769.
18. N'Guyen P.M., Niemeyer E.D. Effects of nitrogen fertilization on the phenolic composition and antioxidant properties of basil (Ocimum basilicum L.). J. Agric. Food Chem. 2008, 56:8685-8691.
19. Urbanczyk-Wochniak E., Fernie A.R. Metabolic profiling reveals altered nitrogen nutrient regimes have diverse effects on the metabolism of hydroponically-grown tomato (Solanum lycopersicum) plants. J. Exp. Bot. 2005, 56:309-321.
20. Acevedo de la Cruz A., Hilbert G., Rivière C., Mengin V., Ollat N., Bordenave L., Decroocq S., Delaunay J.C., Delrot S., Merillon J.M., Monti J.P., Gomes E., Richard T. Anthocyanin identification and composition of wild Vitis spp. accessions by using LC-MS and LC-NMR. Anal. Chim. Acta 2012, 732:145-152.
21. Liang Z.C., Owens C.L., Zhong G.Y., Cheng L.L. Polyphenolic profiles detected in the ripe berries of Vitis vinifera germplasm. Food Chem. 2011, 129:940-950.
22. Im H.W., Suh B.S., Lee S.U., Kozukue N., Ohnsi-Kameyama M., Levin C.E., Friedman M. Analysis of phenolic compounds by high-performance liquid chromatography and liquid chromatography/mass spectrometry in potato plant flowers, leaves, stems and tubers and in home-processed potatoes. J. Agric. Food Chem. 2008, 56:3341-3349.
23. Lewis C.E., Walker J.R.L., Lancaster J.E., Sutton K.H. Determination of anthocyanins, flavonoids and phenolic acids in potatoes. I: Coloured cultivars of Solanum tuberosum L. J. Sci. Food Agric. 1998, 77:45-57.
24. n. J. Agric. Food Chem. 2009, 57:2816-2825.
25. Truong V.D., Deighton N., Thompson R.T., McFeeters R.F., Dean L.O., Pecota K.V., Yencho G.C. Characterization of anthocyanins and anthocyanidins in purple-fleshed sweetpotatoes by HPLC-DAD/ESI-MS/MS. J. Agric. Food Chem. 2010, 58:404-410.
26. Ding S., Dudley E., Plummer S., Tang J., Newton R.P., Brenton A.G. Fingerprint profile of Ginkgo biloba nutritional supplements by LC/ESI-MS/MS. Photochemistry 2008, 69:1555-1564.
27. Zeng G., Xiao H., Liu J., Liang X. Identification of phenolic constituents in radix Salvia miltiorrhizae by liquid chromatography/electrospray ionization mass spectrometry. Rapid Commun. Mass Spectrom. 2006, 20:499-506.
28. Zhang Y., Shi P., Qu H., Cheng Y. Characterization of phenolic compounds in Erigeron breviscapus by liquid chromatography coupled to electrospray ionization mass spectrometry. Rapid Commun. Mass Spectrom. 2007, 21:2971-2984.
29. Fernandez-Panchon M.S., Villano D., Troncoso A.M., Garcia-Parrilla M.C. Antioxidant activity of phenolic compounds: from in vitro to in vivo evidence. Crit. Rev. Food Sci. Nutr. 2008, 48:649-671.
30. Taveira M., Ferreres F., Gil-Izquierdo A., Oliveira L., Valentao P., Andrade P.B. Fast determination of bioactive compounds from Lycopersicon esculetum Mill leaves. Food Chem. 2012, 135:748-755.
31. Iijima Y., Nakamura Y., Ogata Y., Tanaka K., Sakurai N., Suda K., Suzuki T., Suzuki H., Okazaki K., Kitayama M., Kanaya S., Aoki K., Shibata D. Metabolite annotations based on the integration of mass spectral information. Plant J. 2008, 54:949-962.
32. Moco S., Bino R.J., Vorst O., Verhoeven H.A., de Groot J., van Beek T.A., Vervoort J., de Vos C.H.R. A liquid chromatography-mass spectrometry-based metabolome database for tomato. Plant Physiol. 2006, 141:1205-1218.
33. Moco S., Capanoglu E., Tikunov Y., Bino R.J., Boyacioglu D., Hall R.D., Vervoort J., de Vos R.C.H. Tissue specialization at the metabolite level is perceived during the development of tomato fruit. J. Exp. Bot. 2007, 58:4131-4146.
34. Slimestad R., Verheul M. Review of flavonoids and other phenolics from fruits of different tomato (Lycopersicon esculentum Mill.) cultivars. J. Sci. Food Agric. 2009, 89:1255-1270.
35. Vallverdu-Queralt A., Jauregui O., Medina-Remon A., Andres-Lacueva C., Lamuela-Raventos R.M. Improved characterization of tomato polyphenols using liquid chromatography/electrospray ionization linear ion trap quadrupole Orbitrap mass spectrometry and liquid chromatography/electrospray ionization tandem mass spectrometry. Rapid Commun. Mass Spectrom. 2010, 24:2986-2992.
36. Le Bot J., Bénard C., Robin C., Bourgaud F., Adamowicz S. The 'trade-off' between synthesis of primary and secondary compounds in young tomato leaves is altered by nitrate nutrition: experimental evidence and model consistency. J. Exp. Bot. 2009, 60:4301-4314.
37. Royer M., Larbat R., Le Bot J., Adamowicz S., Robin C. Is the C:N ratio a reliable indicator of C allocation to primary and defence-related metabolisms in tomato. Phytochemistry 2013, 88:25-33.
38. Ferreres F., Taveira M., Gil-Izquierdo A., Oliveira L., Teixerira T., Valentao P., Simoes N., Andrade P.B. High-performance liquid chromatography-diode array detection-electrospray ionization multi-stage mass spectrometric screening of an insect/plant system: the case of Spodoptera littoralis/Lycopersicon esculentum phenolics and alkaloids. Rapid Commun. Mass Spectrom. 2011, 25:1972-1980.
39. Zacarés L., López-Gresa M.P., Fayos J., Primo J., Bellés J.M., Conejero V. Induction of p-coumaroyldopamine and feruloyldopamine, two novel metabolites, in tomato by the bacterial pathogen Pseudomonas syringae. Mol. Plant Microbe Interact. 2007, 20:1439-1448.
40. Adamowicz S., Le Bot J., Huanosto Magaña R., Fabre J. Totomatix: a novel automatic set-up to control diurnal, diel and long-term plant nitrate nutrition. Ann. Bot. 2012, 109:309-319.
41. Sawada Y., Akiyama K., Sakata A., Kuwahara A., Otsuki H., Sakurai T., Saito K., Hirai M.Y. Widely targeted metabolomics based on large-scale MS/MS data for elucidating metabolite accumulation patterns in plants. Plant Cell Physiol. 2009, 50:37-47.
42. Strack D., Engel U., Weissenböck G., Grotjahn L., Wray V. Ferulic acid esters of sugar carboxylic acids from primary leaves of rye (Secale cereale). Phytochemistry 1986, 25:2605-2608.
43. Maas M., Petereit F., Hensel A. Caffeic acid derivatives from Eupatorium perfoliatum L. Molecules 2009, 14:36-45.
44. Schwaiger S., Seger C., Wiesbauer B., Schneider P., Ellmerer E.P., Sturm S., Stuppner H. Development of an HPLC-PAD-MS assay for the identification and quantification of major phenolic edelweiss (Leontopodium alpinum Cass.) constituents. Phytochem. Anal. 2006, 17:291-298.
45. Risch B., Herrmann K., Wray V., Grotjahn L. 2'-(E)-O-p-Coumaroylgalactaric acid and 2'-(E)-O-feruloylgalactaric acid in citrus. Phytochemistry 1987, 26:509-510.
46. Elliger C.A., Lundin R.E., Haddon W.F. Caffeoyl esters of glucaric acid in Lycopersicon esculentum leaves. Photochemistry 1981, 20:1133-1134.
47. Strack D., Gross W. Properties and activity changes of chlorogenic acid:glucaric acid caffeoyltransferase from tomato (Lycopersicon esculentum). Plant Physiol. 1990, 92:41-47.
48. Teutschbein J., Gross W., Nimtz M., Milkowski C., Hause B., Strack D. Identification and localization of a lipase-like acyltransferase in phenylpropanoid metabolism of tomato (Solanum lycopersicum). J. Biol. Chem. 2010, 285:38374-38381.
49. Fang N., Yu S., Prior R.L. LC/MS/MS characterization of phenolic constituents in dried plums. J. Agric. Food Chem. 2002, 50:3579-3585.
50. Schoch G., Goepfert S., Morant M., Hehn A., Meyer D., Ullmann P., Werck-Reichhart D. CYP98A from Arabidopsis thaliana is a 3'-hydroxylase of phenolic esters, a missing link in the phenylpropanoid pathway. J. Biol. Chem. 2001, 276:36566-36574.
51. Wolfram K., Schmidt J., Wray V., Milkowski C., Schliemann W., Strack D. Profiling of phenylpropanoids in transgenic low-sinapine oilseed rape (Brassica napus). Phytochemistry 2010, 71:1076-1084.
52. Afzan A., Abdullah N.R., Halim S.Z., Rashid B.A., Semail R.H.R., Abdullah N., Jantan I., Muhammad H., Ismail Z. Repeated dose 28-days oral toxicity study of Carica papaya L. leaf extract in Sprague dawley rats. Molecules 2012, 17:4326-4342.
53. Steffens J.C., Harel E., Hunt M.D. Polyphenol oxidase. Genetic Engineering of Plant Secondary Metabolism 1994, vol. 28:275-312. Plenum Press, New York.
54. Lehfeldt C., Shirley A.M., Meyer K., Ruegger M.O., Cusumano J.C., Viitanen P.V., Strack D., Chapple C. Cloning of the SNG1 gene of Arabidopsis reveals a role for a serine carboxypeptidase-like protein as an acyltransferase in secondary metabolism. Plant Cell 2000, 12:1295-1306.
55. Baumert A., Mock H.P., Schmidt J., Herbers K., Sonnewald U., Strack D. Patterns of phenylpropanoids in non-inoculated and potato virus Y-inoculated leaves of transgenic tabacco plants expressing yeast-derived invertase. Photochemistry 2001, 56:535-541.
56. Keller H., Hohlfeld H., Wray V., Halabrock K., Scheel D., Starck D. Change in the accumulation of soluble and cell wall-bound phenolics in elicitor-treated cell suspension cultures and fungus-infected leaves of Solanum tuberosum. Phytochemistry 1996, 42:389-396.
57. Matsuda F., Hirai M.Y., Sasaki E., Akiyama K., Yonekura-Sakakibara K., Provart N.J., Sakurai T., Shimada Y., Saito K. AtMetExpress development: A phytochemical atlas of Arabidopsis development. Plant Physiol. 2010, 152:566-578.
58. Hanhineva K., Rogachev I., Kokko H., Mintz-Oron S., Venger I., Karenlampi S., Aharoni A. Non-targeted analysis of spatial metabolite composition in strawberry (Fragaria x ananassa) flowers. Phytochemistry 2008, 69:2463-2481.
59. López-Gresa M.P., Torres C., Campos L., Lisón P., Rodrigo I., Bellés J.M., Conejero V. Identification of defence metabolites in tomato plants infected by the bacterial pathogen Pseudomonas syringae. Environ. Exp. Bot. 2011, 74:216-228.
60. van der Rest B., Danoun S., Boudet A.M., Rochange S.F. Down-regulation of cinnamoyl-coA reductase in tomato (Solanum lycopersicum L.) induces dramatic changes in soluble phenolic pools. J. Exp. Bot. 2006, 57:1399-1411.
61. Hagel J.M., Facchini P.J. Elevated tyrosine decarboxylase and tyramine hydroxycinnamoyltransferase levels increase wound-induced tyramine-derived hydroxycinnamic acid amide accumulation in transgenic tobacco leaves. Planta 2005, 221:904-914.
62. Werner C., Hu W., Lorenzi-Riatsch A., Hesse M. Di-coumaroylspermidines and tri-coumaroylspermidines in anthers of different species of the genus Aphelandra. Phytochemistry 1995, 40:461-465.
63. Bassard J.E., Ullmann P., Bernier F., Werck-Reichhart D. Phenolamides bridging polyamines to the phenolic metabolism. Phytochemistry 2010, 71:1808-1824.
64. Le Gall G., DuPont M.S., Mellon F.A., Davis A.L., Collins G.J., Verhoeyen M.E., Colquhoun I.J. Characterization and content of flavonoid glycosides in genetically modified tomato (Lycopersicon esculentum) fruits. J. Agric. Food Chem. 2003, 51:2438-2446.
65. Ruiz A., Hermosin-Gutierrez I., Mardones C., Vergara C., Herlitz E., Vega M., Dorau C., Winterhalter P., von Baer D. Polyphenols and antioxidant activity of calafate (Berberis microphylla) fruits and other native berries from southern Chile. J. Agric. Food Chem. 2010, 58:6081-6089.
66. Slimestad R., Fossen T., Verheul M.J. The flavonoids of tomatoes. J. Agric. Food Chem. 2008, 56:2436-2441.
67. Mirnezhad M., Romero-Gonzalez R.R., Leiss K.A., Choi Y.H., Verpoorte R., Klinkhamer P.G.L. Metabolomic analysis of host plant resistance to thrips in wild and cultivated tomatoes. Phytochem. Anal. 2009, 21:110-117.
68. Báidez A.G., Gómez P., Del Río J.A., Ortuño A. Antifungal capacity of major phenolic compounds of Olea europaea L. against Phytophthora megasperma Drechsler and Cylindrocarpon destructans (Zinssm.) Scholten. Physiol. Mol. Plant Pathol. 2006, 69:224-229.
69. Mathews H., Clendennen S.K., Caldwell C.G., Liu X.L., Connors K., Matheis N., Schuster D.K., Menasco D.J., Wagoner W., Lightner J., Wagner D.R. Activation tagging in tomato identifies a transcriptional regulator of anthocyanin biosynthesis, modification and transport. Plant Cell 2003, 15:1689-1703.
70. Vodopivec B.M., Wang J., Møller A.L., Krake J., Lund T., Hansen P.E., Nielsen S.L. Differences in structure of anthocyanins from the two amphibious plants, Lolebia cardinalis and Nesaea crassicaulis. Nat. Prod. Res. 2013, 27:655-664.
71. Scott J.W., Harbaugh B.K. MicroTom. A Miniature Dwarf Tomato. Florida Agricultural Experimental Station Circular S-370 1989, 1-6.
72. Martí E., Gisbert C., Bishop G.J., Dixon M.S., García-Martínez J.L. Genetic and physiological characterization of tomato cv. Micro-Tom. J. Exp. Bot. 2006, 57:2037-2047.
73. Campos M.L., de Almeida M., Rossi M.L., Martinelli A.P., Litholdo C.G., Figueira A., Rampelotti-Ferreira F.T., Vendramim J.D., Benedito V.A., Peres L.E.P. Brassinosteroids interact negatively with jasmonates in the formation of anti-herbivory traits in tomato. J. Exp. Bot. 2009, 60:4346-4360.
74. Yang D.H., Baldwin I.T., Wu J.Q. Silencing brassinosteroid receptor BRI1 impairs herbivory-elicited accumulation of jasmonic acid-isoleucine and diterpene glycosides, but not jasmonic acid and trypsin proteinase inhibitors in Nicotiana attenuata. J. Integr. Plant Biol. 2013, 55:514-526.
75. Wang M., Liu X., Wang R., Li W., Rodermel S., Yu F. Overexpression of a putative Arabidopsis BAHD acyltransferase causes dwarfism that can be rescued by brassinosteroid. J. Exp. Bot. 2012, 63:5787-5801.
76. Yuan T., Fujioka S., Takatsuto S., Matsumo S., Gou X., He K., Russell S.D., Li J. BEN1, a gene encoding a dihydroflavanol-4-reductase (DFR)-like protein, regulates the levels of brassinosteroids in Arabidopsis thaliana. Plant J. 2007, 51:220-233.
77. Carvalho R.F., Campos M.L., Pino L.E., Crestana S.L., Zsögön A., Lima J.E., Benedito V.A., Peres L.E.P. Convergence of developmental mutants into a single tomato model system: 'Micro-Tom' as an effective toolkit for plant development research. Plant Methods 2011, 7:18.
78. Takahashi H., Shimizu A., Arie T., Rosmalawati S., Fukushima S., Kikuchi M., Hikichi Y., Kanda A., Takahashi A., Kiba A., Ohnishi K., Ichinose Y., Taguchi F., Yasuda C., Kodama M., Egusa M., Masuta C., Sawada H., Shibata D., Hori K., Watanabe Y. Catalog of Micro-Tom tomato responses to common fungal, bacterial, and viral pathogens. J. Gen. Plant Pathol. 2005, 71:8-22.
79. Walker R.L., Burns I.G., Moorby J. Responses of plant growth rate to nitrogen supply: a comparison of relative addition and N interruption treatments. J. Exp. Bot. 2001, 52:309-317.
80. Geny L., Broquedis M. Developmental processes, polyamine composition and content of fruiting cuttings of Vitis vinifera L.: response to nitrogen deficiency. Vitis 2002, 41:123-127.
81. Bryant J.P., Chapin F.S., Klein D.R. Carbon nutrient balance of boreal plants in relation to vertebrate herbivory. Oikos 1983, 40:357-368.
82. Herms D.A., Mattson W.J. The dilemma of plants: to grow or defend. Q. Rev. Biol. 1992, 67:283-335.
83. SARK{proportion}IPT tobacco plants. Plant Physiol. Biochem. 2012, 57:231-237.
84. Serapiglia M.J., Minocha R., Minocha S.C. Changes in polyamines, inorganic ions and glutamine synthetase activity in response to nitrogen availability and form in red spruce (Picea rubens). Tree Physiol. 2008, 28:1793-1803.
85. Sung H.I., Liu L.F., Kao C.H. The decrease in polyamine levels is not associated with growth inhibition in suspension-cultured rice cells under nitrogen deficiency. Biol. Plant. 1995, 37:213-217.
86. von Roepenack-Lahaye E., Newman M.A., Schornack S., Hammond-Kosack K.E., Lahaye T., Jones J.D.G., Daniels M.J., Dow J.M. p-Coumaroylnoradrenaline, a novel plant metabolite implicated in tomato defense against pathogens. J. Biol. Chem. 2003, 278:43373-43383.
87. Onkokesung N., Gaquerel E., Kotkar H., Kaur H., Baldwin I.T., Galis I. MYB8 controls inducible phenolamide levels by activating three novel hydroxycinnamoyl-coenzyme A:polyamine transferases in Nicotiana attenuata. Plant Physiol. 2012, 158:389-407.